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Bacterial Microbiome in Wild-Caught Anopheles Mosquitoes in Western Thailand

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Bacterial Microbiome in Wild-Caught Anopheles Mosquitoes in Western Thailand fmicb-11-00965 May 19, 2020 Time: 19:5 # 1 ORIGINAL RESEARCH published: 21 May 2020 doi: 10.3389/fmicb.2020.00965 Bacterial Microbiome in Wild-Caught Anopheles Mosquitoes in Western Thailand Krajana Tainchum1,2†, Chloé Dupont3,4†, Theeraphap Chareonviriyaphap2, Estelle Jumas-Bilak3,4, Michael J. Bangs2,5 and Sylvie Manguin3* 1 Agricultural Innovation and Management Division, Faculty of Natural Resources, Prince of Songkla University, Songkhla, Thailand, 2 Center for Advanced Studies for Agriculture and Food, KU Institute for Advanced Studies, Kasetsart University, Bangkok, Thailand, 3 HydroSciences Montpellier, Institut de Recherche pour le Développement, CNRS, Université Montpellier, Montpellier, France, 4 Centre Hospitalier Universitaire, Laboratoire d’Hygiène Hospitalière, Montpellier, France, 5 Public Health & Malaria Control, PT Freeport Indonesia/International SOS, Kuala Kencana, Indonesia Among the complex microbial community living in the mosquito midgut, some bacteria (e.g., Enterobacter spp.) can deliver effector molecules with anti-Plasmodium effects suppressing the development of malaria parasites (Plasmodium falciparum) before the öokinete can penetrate the mosquito midgut epithelium. Despite knowledge of this phenomenon, only a few studies have defined the diversity of microbiota in wild-caught adult Anopheles species. The objective of this study was to analyze and compare Edited by: the bacterial microbiota in different Anopheles species, including representatives of Josué Martínez-de la Puente, Consejo Superior de Investigaciones the primary malaria vectors in western Thailand. Wild female Anopheles species were Científicas (CSIC), Spain sampled from malaria-endemic areas in Tak and Mae Hong Son provinces near the Reviewed by: Thai-Myanmar border. Midgut/abdominal bacterial diversity was assessed by examining Guido Favia, the 16S rRNA gene, V3 hypervariable region, using PCR-Temporal Temperature Gel University of Camerino, Italy Rajnikant Dixit, Electrophoresis (PCR-TTGE) profiling and sequence analysis. A total of 24 bacterial National Institute of Malaria Research, genera were identified from eight Anopheles species. Five bacterial genera were India newly reported in Anopheles mosquitoes (Ferrimonas, Megasphaera, Pectobacterium, *Correspondence: Sylvie Manguin Shimwellia, and Trabulsiella). Five genera, including Megasphaera, were detected [email protected] exclusively in a single-malaria (Plasmodium vivax) infected Anopheles minimus and not †These authors have contributed observed in other non-infected mosquitoes. The use of PCR-TTGE provides the first equally to this work characterization of the midgut bacterial microbiome present in wild adult Anopheles in Specialty section: Thailand. Evidence that microbiota might impact pathogen development (suppression) This article was submitted to in Anopheles and thereby reduce the risk of pathogen transmission deserves more Infectious Diseases, studies to describe the presence and better understand the biological role of bacteria in a section of the journal Frontiers in Microbiology natural mosquito populations. Received: 20 December 2019 Keywords: Anopheles mosquitoes, malaria, bacterial microbiota, biodiversity, Thailand Accepted: 22 April 2020 Published: 21 May 2020 Citation: INTRODUCTION Tainchum K, Dupont C, Chareonviriyaphap T, Jumas-Bilak E, Despite significant progress in the control of malaria throughout the country, Thailand remains Bangs MJ and Manguin S (2020) Bacterial Microbiome in Wild-Caught malaria-endemic, particularly along the international borders with Cambodia, Lao PDR, Malaysia, Anopheles Mosquitoes in Western and Myanmar (DDC, 2018). The vast majority of recorded malaria cases, primarily Plasmodium Thailand. Front. Microbiol. 11:965. vivax (73%) and Plasmodium falciparum (18%), occur along the Thai-Myanmar border (70–80%), doi: 10.3389/fmicb.2020.00965 especially in Tak and Mae Hong Son provinces (DDC, 2018). Of the 79 recognized Anopheles species Frontiers in Microbiology| www.frontiersin.org 1 May 2020| Volume 11| Article 965 fmicb-11-00965 May 19, 2020 Time: 19:5 # 2 Tainchum et al. Bacterial Microbiota of Anopheles Mosquitoes From Thailand present in Thailand, the most important malaria vectors microbiota in the mosquito midgut and abdomen, primarily include two sibling species in the Dirus Complex (Anopheles Gram-negative bacterial rods, including Serratia marcescens, baimaii Sallum & Peyton, and Anopheles dirus Peyton & Klebsiella ozaenae, Pseudomonas aeruginosa, Escherichia coli, and Harrison), Anopheles minimus Theobald, Anopheles aconitus Enterobacter spp. (Manguin et al., 2013). Other studies have Dönitz, and three members of the Maculatus Group (Anopheles reported the majority of adult mosquito midgut microbiota were maculatus Theobald, Anopheles pseudowillmori [Theobald], Gram-negative species in the phylum Proteobacteria (Tandina and Anopheles sawadwongporni Rattanarithikul & Green) et al., 2016; Zoure et al., 2020). At least three mosquito- (Tananchai et al., 2019). specific bacterial species have been isolated from the midgut The malaria sporogonic cycle begins when a female mosquito of African malaria vectors in the Gambiae Complex, including ingests infective-stage (gametocytes) Plasmodium parasites from Thorsellia anophelis, Janibacter anophelis (Kampfer et al., 2006) the blood of an infected human host. The ingested parasites and Elizabethkingia anophelis (Kampfer et al., 2011). Despite undergo syngamy to create motile stage öokinetes that penetrate a large amount of work done on malaria vectors over many the mosquito midgut to become oocysts. The oocyst gradually decades, few studies have examined the natural diversity of enlarges as parasites multiply to produce many sporozoites. microbiota in adult mosquitoes (Manguin et al., 2013; Bassene Once released from the oocyst, sporozoites migrate to the et al., 2018). Therefore, the objective of this study is to use salivary glands to await transmission to another host via a a sensitive molecular method to evaluate the natural bacterial mosquito bite. Although many Plasmodium gametocytes can be diversity in wild-caught adult Anopheles in a malaria-endemic ingested during a single blood-feeding, only a small fraction region of western Thailand. typically develop to form oocysts (Leroy et al., 2014). The reason for this sharp decrease in potential infection density is multifactorial (genetic and non-genetic) and in large part influenced by the parasite-vector species relationship and MATERIALS AND METHODS individual mosquito susceptibility (competence) to Plasmodium infection allowing successful sporogonic development of the Ethics Statement parasite while minimizing significant adverse effects on mosquito Human use protocol (human-landing collections) for this study fitness (survival, fecundity, etc.) (Black and Severson, 2005; was reviewed and approved by the Ethical Research Committee, Lefevre et al., 2013). One area of research on this relationship has Chulalongkorn University, Bangkok, Thailand (No. 0961/56). been the modulating effects linked to certain naturally occurring microbiota in the midgut and abdomen of mosquitoes that can suppress or prevent Plasmodium development (Cirimotich et al., Mosquito Collections and Species 2011b). In particular, the role of enterobacteria that influences Identification parasite development and transmission has been investigated In 2011, adult Anopheles mosquitoes were collected from in Anopheles mosquitoes. Additional investigations on this two hypoendemic malaria locations along the Thai-Myanmar phenomenon may help to develop novel methods involving border in Tak and Mae Hong Son provinces, respectively bacterial symbionts to arrest malaria from vector to host. (Figure 1), using a standard human-landing collection technique Symbiotic bacteria, such as Pantoea agglomerans and Asaia (Tainchum et al., 2014). Table 1 provides geographic locations, spp., have been successfully transformed to express anti-malaria prevailing climatic factors, environment biotype, and crude molecules (anti-plasmodia effector proteins) that render host malaria incidence rate (2010–2012). The abundance of the mosquitoes refractory to malaria infection (Favia et al., 2008; primary malaria vectors, An. minimus, An. dirus complex, and Damiani et al., 2010; Wang et al., 2012); in effect, becoming An. maculatus group, by month of collection (from February a paratransgenic means for preventing malaria transmission to November 2011) and location, is presented in Figure 2. (i.e., transmission-blocking strategy) (Doumbo et al., 2018). Live mosquitoes were initially sorted using discriminating Engineered P. agglomerans strains can inhibit up to 98% of morphological criteria for species, complex or group level P. falciparum development in infected mosquitoes (Riehle et al., identification (Rattanarithikul et al., 2006). For further mosquito 2007). Enterobacter (Esp_Z) is shown to inhibit öokinete, oocyst, identification, Anopheles specimens were assayed using the and sporozoite formation of P. falciparum in Anopheles gambiae appropriate allele-specific PCR technique by species complex by up to 99% (Cirimotich et al., 2011b). Co-infections with or group (Tainchum et al., 2014). Each mosquito was divided Serratia marcescens and P. vivax in Anopheles albimanus have in two parts, head-thorax for mosquito species identification resulted in only 1% of mosquitoes being able to develop oocysts and detection of malaria (Plasmodium) infection, and abdomen and complete sporogonic development
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